Management breaks the natural productivity-biodiversity relationship in forests and grassland: an opinion
© The Author(s). 2018
Received: 7 August 2017
Accepted: 14 December 2017
Published: 24 January 2018
Two approaches mark the difference between the “ecological” and “agricultural” view of the biodiversity/growth relation. In ecology the trend is averaged by taking monocultures of all species as baseline to evaluate mixtures. This contrasts the “agricultural” view focusing on the most productive species or species combination as baseline to evaluate mixtures. The present study investigates the change of highest rates (maximum) productivities in grasslands and forests with increasing plant (or tree) diversity, and compares these with the average response.
We base our analysis on existing published datasets relating the growth of plant stands (growth rate per land area) to the diversity on the same plot. We use a global dataset (Ellis et al. 2012 and MODIS-data, see Fig. 1), the grassland experiment in Jena (Buchmann et al. 2017), the regional study on forests in Romania and Germany by Bouriaud et al. (2016), and data from the German National Forest inventory (BWI 3, see Fig. 3). In all cases the average response of growth to changes in biodiversity as well as the boundary line of the maximum values was calculated.
In both vegetation types a decreasing trend of maximum productivity with any added species emerges, contrasting the average trend that was positive in grassland, but absent in forests. The trend of maximum values was non-significant in grasslands probably due to the fact that not all combinations of species mixtures were available. In temperate forests, maximum productivity decreases significantly by about 10% in regional studies and by 8% at national scale with each added species. Maximum biomass per area was the same for managed and unmanaged conditions. A global assessment of NPP and biodiversity could also not confirm a general positive biodiversity-productivity relationship.
Managed grasslands and forests reach highest productivity and volumes at low diversity. Also globally we could not confirm a biodiversity effect on productivity. Despite this, for long-living organisms, such as trees, the incentive for land managers exists to reduce the risk of failure due to climate extremes and diseases by taking a loss in productivity into account and to actively maintain a mixture of species.
Mankind faces an increasing number of conflicting demands for maintaining global integrity. There is the need for mitigating climate change, the demand for maintaining global diversity, and the necessity to supply an ever increasing amount of biomass for human needs of food, wood, energy and fiber. In this context, the observation that biomass production can be increased by increasing plant diversity is highly important. Hector et al. (1999) summarized the results from a European Grassland Experiment by the simple equation, namely that doubling plant diversity increases biomass production of grasslands by 20%. However, despite an overwhelming confirmation of this observation from other ecosystems (Scherer-Lorenzen in Schulze et al. 2017), the acceptance by land-users in agriculture and forestry remains low. Monocultures remain the main source for food and fiber worldwide perhaps of conflicting interpretations of the same results, or because of practical reasons, since maintaining diversity can be very work-demanding.
In the following we try to explore the basis for these opposing views, namely the demand for increasing biomass production via diversity and the resilience by land-users to discard monocultures. In this process, we should be aware, that the relation between biomass production and diversity is not direct, but mediated by numerous parameters, including human management, and by variations in site conditions. In an initial step we will evaluate global distributions of diversity and productivity in order to re-inspect in a second step grassland and forest experiments.
In this study we re-asses existing data by Bouriaud et al. (2016), Buchmann et al. (2017), Schall et al. (2017) and Liang et al. (2016) specifically in terms of biodiversity effects. In the past, the productivity/diversity relations were studied with a focus on the average change of productivity with plant species numbers. In most cases, an increase with diversity was observed and interpreted by the effects of selection and complementarity (Loreau and Hector 2001). However, Schmidt et al. (2008) already pointed out that average (or 0.5 percentile) functions overestimate the diversity effects due to high numbers of monocultures in experimental assembles. In the present study, we try to overcome the problems of non-normal distributions of data, by inspecting the maximum value or values of productivity at each level of species number, and we compare this function with the average diversity response. The statistical problem remains that the sample size changes with the level of species number, but taking the maximum values can avoid unwanted effects of management on maximum productivity.
Results and Discussion
Global diversity and productivity
Obviously, the NPP-diversity relation is not linear across the range of diversity, where the global distribution of diversity is left-skewed towards low diversity. The increasing variation and the final decline of NPP with diversity may be explained by the fact, that many hotspots are located in alpine and semi-arid regions.
The relation of NPP and global diversity does not allow an assessment of the effects of a loss of species. The effect on NPP may be detrimental, if a dominant species is lost (e.g. Picea abies during forest decline by SO2 emissions). In this case NPP may collapse despite high diversity at the pixel level. On the contrary, if an auxiliary species is lost (e.g. Ulmus ssp., by Duch elm disease) there may be no effect on NPP. Therefore, in the following we try to separately assess the NPP productivity relations for grasslands and for forests at greater detail.
The data-cloud shows a significant increase of average biomass with increasing plant species number, explaining 21% of the variation. The increase is caused by a selection and by a complementarity effect (Loreau and Hector 2001). However, there is a tendency for more data points at low diversity (monoculture of each species as reference) than at high diversity, which may affect the slope of the NPP/diversity relation (Schmid et al. 2008). The analyses of Buchmann et al. (2017) of the mechanisms of this positive relation shows that biomass-production via diversity is mainly determined by the availability of nitrogen, where nitrogen is supplied by legumes. In managed grasslands nitrogen is added by fertilizer.
Neither the grassland experiments nor the ambient semi-natural grasslands contain all possible species combinations. Therefore we try to assess the diversity effect in a reverse approach, by viewing selectively the maximum rates at each density level, even though the problem exists that not all species combinations contain the species of highest productivity (a kind of negative selection effect). The highest biomass values (5% percentile) shows decreasing biomass with diversity (r2 = 0.31), but the number of available data is too small to be significant. The maximum biomass was observed at 10 species mixtures. Biomass of a single species in a 3 species mixture may be as high as the species mixture of 17 and more species, as known from fertilized meadows (Buchgraber and Grindl 2004). The data set does not contain a high-yielding monoculture. The average loss in maximum productivity is 0.5% loss with each absent species, but it remains unclear, if the initial response is linear. A positive effect of species mixtures apparently remains at low species numbers, most likely by over-yielding.
The two approaches mark the main difference between the “ecological” view of the average trend taking monocultures of all species as baseline, and the “agricultural” view focusing on highest productivity. Also, agriculturist would be interested to know, which features result in highest biomass production. We will not evaluate the two approaches but point at genuine differences. In the case of the Jena-Experiment, the highest NPP was reached by Onobrychis viciifolia (esparsette) as dominant species with few additional subdominant species. Onobrychis also contributes to a large extent to the high NPP at experimental species mixtures. It is a nitrogen fixing species. At the same time, it grows tall and forms a dense canopy of sun-leaves that out-shade most competitors. Obviously, maintaining high yielding grasslands with few species requires additional management (Buchgraber and Grindl 2004).
Relations between forest growth and tree diversity are difficult to assess because, in many studies only stand volumes and not growth are documented, and the main species of the canopy and not all species are recorded. Therefore, we restrict our analysis to temperate zone central European forests where all data are available.
The inventory study in a temperate European forest reached 9 tree species per inventory plot as highest level of tree diversity on 1000 m2 plots. We would expect that this number would be higher in East Asia or North America having higher regional tree diversity (Schulze et al. 2015). In order to make sure that the tree species number reached in Figs. 3 and 4 is representative, we analyzed the data of Schall et al. (2017) on 1 ha plots in the same region of Germany, but confined to deciduous forest (See Additional file 1: Figure S3). This study reached 8 tree species as maximum tree diversity. Thus, the small inventory plots and the relatively low level of tree diversity are representative for European forests.
Apparently, in forests, tree diversity is maintained either by disturbances, including human management (Reich et al. 2001; Schulze et al. 2009), or by open canopies when environmental conditions are limiting, and it could be both, namely that NPP determines diversity (Reich et al. 2001) or that species composition determines NPP (Schulze et al. 2009).
Global biodiversity data
It is of interest to note that the full dataset of Liang et al. (2016) shows a distinct peak at low and at intermediate diversity (see Additional file 1: Figure S2). The full dataset apparently contains a mixture of volumes and growth rates and thus remains difficult to interpret. Nevertheless, it remains interesting to see that an envelope function (of volumes) would decline with diversity, indicating reduced stand growth with increasing diversity. There appears to be a second lower peak at intermediate diversity.
The data indicate that the maximum growth rate of specific monocultures and mixtures is higher than the average diversity effect on productivity. This may be taken as the main incentive of land-users to using monocultures. In forests the loss in maximum productivity is about 10% for each added species, and this is less than the potential gain of average productivity in a random mixture. Highly productive monoculture-trees are also very strong competitors (e.g. Picea and Fagus) and keeping admixture species alive requires frequent interventions by management.
Food industry and bio-economy are additional strong drivers for monocultures because of a demand for a uniform supply of substrate wanted for uniform products. This is even true for forestry, where saw mills are specialized to use specific tree species only. Thus, from the economic side there are few incentives to promote species mixtures.
Opposite to the incentives for monocultures in managed systems, there are also ecological incentives for species mixtures, especially in long-lived forests. A mixture of species results in reduced risk against environmental extreme events (wind-throw) and diseases (insects). It also buffers the temporal variations of climate on productivity (Jucker et al. 2014; Isbell et al. 2015). Thus, in temperate forests, a species mixture is anticipated in modern forestry, but the level of mixture is generally low.
Estimates of the cost of losses of species cannot be based on the average growth/biodiversity function, neither at global nor at local scale, but must contain the fact, that management will select the most productive species or species combination, which produce biomass beyond the level of the growth/biodiversity function.
This study does not intend to clarify the ultimate causes for correlations between NPP and biodiversity or NPP and biodiversity, but to point out that by management NPP can be increased beyond the level offered by natural mixtures of species.
We like to thank Prof Dr. Alexandra Weigelt, Dr. Anne Ebeling, Dr. Tina Buchmann for making the grassland dataset available. These data were collected in the context of the Jena Experiment with Prof. Dr. Nico Eisenhauer, Prof. Dr. Wolfgang Weisser, and Prof. Dr. Berhard Schmid as PIs, and we thank these persons for maintaining this project. We thank Uli Pruschitzki and Lulian Iulian Dănilă for organizing the forest inventories.
EDS: wrote the 1st draft and all revisions of this paper, OB: analyzed the Romanian forest inventory date, UW: developed the global analysis of NPP vs. biodiversity, CR: analyzed the grassland data, DH analyzed the German forest inventory data, FK contributed the data of the German national forest inventory; PS made statistical analyses; FK supplied the data of the German National Forest Inventory. All authors jointly discussed this broad dataset, and agreed to the final version.
The authors declare that they have no competing interest.
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